479
Indications of competition between non-indigenous round goby
and native flounder in the Baltic Sea
Agnes M. L. Karlson, Gustaf Almqvist, Krzysztof E. Skóra, and Magnus Appelberg
Karlson, A. M. L., Almqvist, G., Skóra, K. E., and Appelberg , M. 2007. Indications of competition between non-indigenous round goby and native
flounder in the Baltic Sea. – ICES Journal of Marine Science, 64: 479 – 486.
The Ponto-Caspian round goby (Neogobius melanostomus) was introduced to the Gulf of Gdańsk, southern Baltic Sea, in the late
1980s, and it has now become the dominant demersal fish species in shallow water. This study aimed to assess diet preferences
and the degree of diet overlap between the round goby and the native flounder (Platichthys flesus). Results from time-series of
stomach contents and stable isotope analyses of wild-caught fish, together with prey preference experiments carried out in the laboratory, showed that the two species consumed similar species and sizes of prey. The similarities in diet suggest potential for food
competition. Catch data showed both reverse depth distributions of round goby and flounder when round gobies were abundant
and that the abundances of the two species were negatively correlated. The diet overlap between small flounders and round
gobies was greatest when goby abundance was least, suggesting that abundance of round gobies may restrict flounder habitat utilization and, therefore, also food availability to the latter. Therefore, round gobies may have a negative influence on the commercially
important flounder.
Keywords: diet overlap, diet preference, invasive species, ontogenetic diet shifts, stable isotopes.
Received 5 July 2006; accepted 23 December 2006; advance access publication 22 February 2007.
A. M. L. Karlson and G. Almqvist: Department of Systems Ecology, Stockholm University, SE –106 91 Stockholm, Sweden. K. E. Skóra: Hel Marine
Station, Poland Institute of Oceanography, University of Gdańsk, 84 –150 Hel, Poland. M. Appelberg: Institute of Coastal Research, Swedish Board of
Fisheries, Box 109, SE –740 71 Öregund, Sweden. Correspondence to G. Almqvist: tel: þ46 8161059; fax: þ46 8158417; e-mail: [email protected]
Introduction
As a consequence of increased global transport, the number of
non-indigenous species is rapidly increasing in coastal areas
around the world (Carlton, 1996; Ruiz et al., 1997), where they
can affect native species and alter ecosystem functioning (Lodge,
1993; Ruiz et al., 1997; Mack et al., 2000). This may result in economic damage to fisheries, tourism, and other industries (Ruiz
et al., 1997; Leppäkoski, 2002). Dramatic ecological effects on
native fish through direct predation by non-indigenous fish
species has been observed in Lake Victoria and Lake Michigan
(Wells and McLain, 1972; Witte et al., 1992). Negative ecological
effects of competition are more difficult to demonstrate, and
this perhaps is the reason why competition is considered to be a
less serious consequence of invasions (Lodge, 1993; Williamson,
1996). However, competition is an important factor that structures
communities, and resource partitioning is an important mechanism that allows species to coexist (Piet and Guruge, 1997).
In general, habitat and diet are the most important niche
dimensions separating coexisting fish species (Schoener, 1974;
Ross, 1986); both high and low overlap in these dimensions
could be indicative of competition (Ebeling and Hixon, 1991;
Hansson, 1995; Begon et al., 1996; Horta et al., 2004; Raborn
et al., 2004). When species that have not co-evolved start to interact, the risk of competition increases, and non-indigenous fish
species may compete directly with native fauna for resources
(Moyle and Light, 1996; Vander Zanden et al., 1999; Balshine
et al., 2005). The round goby (Neogobius melanostomus) is a
demersal benthivore originating in the Ponto-Caspian region.
# 2007
In the late 1980s, it entered the Gulf of Gdańsk, Southern Baltic,
the Laurentian Great Lakes, North America, and the Moscow
River, Russia, in ballast water (Sokolov et al., 1989; Jude et al.,
1992; Skóra and Stolarski, 1993). In the Gulf of Gdańsk, the area
round gobies occupy overlaps with that of the native flounder
(Platichthys flesus), which also feeds on benthic fauna (Mulicki,
1947; Molander, 1964; Aarnio and Bonsdorff, 1997; Ostrowski,
1997, Rzeznik 1997), and concerns have been raised that the
round goby may be outcompeting flounder for both food and
space (Skóra and Rzeznik, 2001; Wandzel, 2003; Corkum et al.,
2004). Notwithstanding, comparable studies of diet and habitat
have not been conducted for the two species.
Here we assess the spatio-temporal overlap, and diet preferences and overlap between round goby and native flounder by a
combination of gillnet fishing, stomach content analyses, stable
isotope analyses, and laboratory experiments conducted during
summer 2004 in the Gulf of Gdánsk.
Material and methods
Study area and sampling
Fish were sampled off Oksywie (548330 N 188330 E), during June
(7–10), July (17–20), and September (1–3) 2004 (Figure 1).
Fishing grounds off Oksywie are located at the border of Puck
Bay, a vast, shallow area with a bottom characterized by a
mixture of sand, clay, gravel, and boulders (Mojski et al., 1995).
There, round goby, followed by flounder, were the most abundant
fish species during July and August 2003 (GA, pers. obs.). The
study area started some 200 m from shore (water depth 3 m)
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480
A. M. L. Karlson et al.
Figure 1. Gulf of Gdańsk, showing the sampling site outside Oksywie. Inset shows the Baltic Proper, with the rectangle marking the area of
interest.
and extended 2.7 km out to a depth of 13 m. Four fishing stations
(at 3, 7, 10, and 13 m) were established using fixed coordinates,
and 20, 19, and 16 nets were distributed at the stations in June,
July, and September, respectively. In June, both surface and
bottom temperature decreased with distance from shore, at the
surface from 10.68C (3 m station) to 9.08C (13 m) and at the
bottom from 10.68C (3 m) to 5.88C (13 m). In July and
September, the water column was almost homothermic, at
16.1 + 0.98C and 17.4 + 0.38C (mean + s.d.), respectively.
Salinity was 6.9 for all periods and depths.
Fish were collected using Nordic coastal survey nets (45 m long,
1.8 m deep, divided into nine sections with bar mesh sizes of 10,
12, 15, 19, 24, 30, 38, 47, and 60 mm). The nets were set overnight
(for about 10 h) and covered the periods of dusk and dawn, when
both species are thought to feed (Pihl, 1982; Janssen and Jude,
2001). Catch per unit effort (cpue) was calculated for each
fishing station (3, 7, 10, and 13 m) as the average number of fish
caught per net. Total length was recorded to the nearest millimetre
and weight to the nearest 0.1 g for all round gobies and flounders.
The digestive tracts were immediately dissected out and preserved
in 90% ethanol for later analysis. To compare size classes of round
gobies and flounders, we established gape size (maximum height
of gape, measured with a slide calliper without tension) to body
length regressions. Corresponding size classes (small, medium,
and large) have similar gape size, although body length differs
(Table 1).
Stomach content analyses and estimates of diet overlap
Guts and stomachs from 323 round gobies and 209 flounders from
all depths were analysed (Table 2). All prey in the digestive tract
were identified to the lowest possible taxon under a stereo microscope (10 magnification). The number of food components was
determined for each stomach and, taking into consideration the
extent of digestion, e.g. broken bivalves could be approximately
reconstructed, their maximum lengths were measured with a
slide calliper. Shell-free (not to overestimate the importance of,
e.g. bivalves) dry weights of the various food components were
estimated using conversion factors from the literature (Ankar
and Elmgren, 1976; Evans, 1977; Brey et al., 1988; Furman and
Crisp, 1989). Prey other than those shown in Table 2 constituted
a negligible part of the stomach contents and were not included
in the analyses. Diet overlap was estimated with Morisita’s index
(C ) (cf. Horn, 1966; Cortés, 1997):
C¼
2SXi Yi
;
SXi2 þ Yi2
where Xi and Yi are the proportions of the ith food category
(Table 2) in the diet of species X and Y, respectively. An index of
0 means total dissimilarity of the diet, and a value of 1 represents
identical stomach contents; according to Zaret and Rand (1971),
the overlap is ecologically significant if the value is 0.6.
Stable isotope analysis
As a complement to stomach analyses, muscle tissue from each size
class of each species was analysed for stable nitrogen isotopes.
Stable isotopic signatures reflect long-term (weeks –years) diet
composition (Hobson, 1999), whereas stomach contents analysis
Table 1. Gape size (mm) and corresponding total fish length (mm)
per size class.
Size
Gape size
Round goby
Flounder
Small
,14.5
60
–120
100
–120
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .
Medium
14.5
–17
120
–140
200
–250
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .
Large
.17
.140
.250
Categorization based on regression analyses: flounder: r 2 ¼ 0.955,
F1,29 ¼ 597.21, p , 0.0001; round goby: r 2 ¼ 0.956, F1,45 ¼ 945.87,
p , 0.0001.
481
Competition between non-indigenous round goby and native flounder in the Baltic
Table 2. Diet composition (shell-free dry weight, %) from stomach analyses.
Species
Size
n
Month
%
Dry weight
%
%
%
%
%
%
%
%
%
%
empty
(mg)
Myt.
Mac.
Car.
Mya
Bal.
Hyd.
Ner.
Cor.
Gam.
Gas.
Rg
S
June
35
40
19.6
30.9
1.7
0
0
0
39.3
28.1
0
0
0
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Rg
S
July
42
24.4
22.1
30.9
0.8
0
0
0.3
19.2
48.9
0
0
0
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Rg
S
September
70
26.1
8.3
13.9
15.3
22.9
0.8
4.6
31.3
11.1
0
0
0
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Rg
M
June
42
23.8
30.0
36.0
5.8
2.8
0
0.1
38.2
16.0
0
1.0
0
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Rg
M
July
17 33.3
17.9
49.3
2.2
0
0
8.5
12.6
27.5
0
0
0
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Rg
M
September
39
5
22.3
36.6
19.6
9.7
0.1
4.0
22.8
7.3
0
0
0
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Rg
L
June
35
48.6
39.8
41.6
9.5
0.4
0
0.6
24.5
21.2
0
2.3
0
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Rg
L
July
22
40.9
17.8
34.4
21.9
0
0
0.4
39.3
0
0
4.0
0
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Rg
L
September
21
4.8
82.2
75.4
12.7
0.3
0
0.2
6.6
0.1
0
0
4.8
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Fl
S
June
16 43.8
317.9
0.1
56.6
0
0
0.2
11.1
32.0
0
0
0
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Fl
S
July
19
47.4
8.6
20.0
41.0
0
0
0.0
19.2
19.7
0
0
0
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Fl
S
September
37
27
43.9
0
14.5
18.4
0.1
0.3
7.8
35.0
24.0
0
0
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Fl
M
June
17
17.6
94.3
9.6
49.3
9.0
0
0.0
10.2
21.8
0
0
0
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Fl
M
July
25 20.8
39.2
3.5
63.3
5.0
0
5.1
1.3
17.7
4.0
0
0
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Fl
M
September 30 26.7
116.0
4.6
40.9
6.4
1.1
0.1
3.2
16.7
27.1
0
0
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Fl
L
June
20
10
576.9
10.2
56.9
0.0
0
6.6
0.0
16.4
0
0
9.8
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Fl
L
July
18 50
271.2
14.4
62.2
3.5
0.0
0.1
2.1
6.4
5.1
0
6.3
. . . . . . . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . .. . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . .. . . . . . . . . . .
Fl
L
September 17 23
307.9
10.9
56.7
11.3
0.0
0
0.3
8.9
7.8
0
4.0
From left, species (round goby and flounder), size class (small, medium, and large), month, number of fish analysed, n, percentage of fish with empty
stomachs, total dry weight of stomach contents, and the food items in terms of percentage: Myt, Mytilus edulis; Mac, Macoma balthica; Car, Cardium sp.;
Mya, Mya arenaria; Bal, Balanus improvisus; Hyd, Hydrobia; Ner, Nereis diversicolor; Cor, Corophium sp.; Gam, Gammarus sp.: Gas, Gasterosteus aquelatus.
indicates intake over the previous few hours. Nitrogen isotopic
composition is usually expressed in per mil deviations (d 15N)
between the isotope ratio in a sample and that of atmospheric
N2, according to the formula
15
d N¼
15
Nsample =14 Nsample
15 N =14 N
air
air
!
1
103 :
Samples for isotope analyses (a 2 –3 cm piece of muscle from just
behind the head, above the lateral line) were excised immediately
after capture (Hansson et al., 1997), from five random specimens
(in July, only three) of each species, size class, and sampling
period. The samples were dried at 508C, homogenized with a
mortar and pestle, transferred to foil capsules (1 + 0.2 mg), and
analysed for d 15N relative abundance by mass spectrometry at
the University of California, Davis Stable Isotope Facility.
Prey preference
Fish and mussels for prey preference experiments were collected at
the beginning of July off Hel Marine Station, at the tip of the Hel
Peninsula (Figure 1). Fish were acclimatized and starved for a
week before the experiment. In all, 60 fish were selected for the
experiment (n ¼ 10 per size class and species). They were placed
individually in 35 cm high, 40 90 cm glass aquaria, filled to
75% with seawater flow-through (at natural temperature and salinity regimes around 178C and 6.9), a 2 cm sieved (mesh size
1 mm) layer of sand on the bottom, and a stone (the size of a
fist) as refuge. For food, the two most abundant (Wiktor, 1985)
mussel species in the area, Macoma balthica and Mytilus edulis,
were collected by trawl, measured with a slide calliper, and
divided into three size classes: small (3–6 mm), medium (7 –
12 mm), and large (.12 mm). An hour before addition of the
fish, eight mussels of each species and size class (48 in total)
were distributed randomly on the bottom of each aquarium.
The outer walls of the aquaria were covered with black plastic
film to reduce visual stress. This was important, because flounders
are mainly visual feeders (Mattila and Bonsdorff, 1998). Round
gobies can forage in total darkness using their complete lateral
line system (Fuller et al., 2006), but probably also use their welldeveloped eyes (Jude, 1993) to search for food. Fish were
allowed to forage for 18 h, including both dusk and dawn
periods, imitating the natural light regime. At the end of each
experiment, the sand was sieved and all mussels retrieved were
again measured and assigned to a size class. Non-feeding fish
(mainly large flounders) were excluded from the analyses
because they were assumed to respond negatively to laboratory
conditions.
Food selectivity was calculated using Manly’s a (Manly, 1974;
Chesson, 1978, 1983; Swenson and McCray, 1996):
ðdi =Ni Þ
;
ai ¼ Pk
j¼1 ðdi =Ni Þ
where i is the prey type (mussel species and size class), k the
number of prey types in the experiment, di the number (or proportion) of prey of type i in the diet sample, and Ni is the
density (or proportion) of prey type i in the environment. For
the analysis, k ¼ 6, because six prey types were used (two species
of mussel, three size classes). Values of a range from 0 (complete
avoidance) to 1 (complete preference). When ai . 1/k there is
selection for, and when ai , 1/k there is selection against, prey
i. When a ¼ 1/k, the predator is feeding randomly, and the composition of the diet simply reflects the availability of prey in the
environment.
482
A. M. L. Karlson et al.
Data processing and statistics
When possible, we used analysis of variance (ANOVA) to test for
differences among species, size classes, and depths. If transformed
data failed assumptions of normality or equal variance, nonparametric tests were used (Kruskal–Wallis, Mann–Whitney
U-test). When estimating the depth distribution of species, data
from stations of similar depth were merged to generate sufficient
replicates (number of nets per depth), when appropriate.
Similarly, when calculating diet overlap, fish from all depths
were merged to obtain a sufficiently large data set, because
empty stomachs (Table 2) reduced the number of replicates per
size class. All statistical tests were made with STATISTICAw
software.
Results
Depth distributions of round gobies and flounders
The cpue of round gobies and flounders differed significantly
among sampling periods and depths (Figure 2). In June
(Figure 2a), flounders were abundant only at 13 m. The cpue of
round goby was significantly higher (Mann –Whitney U-test,
n ¼ 19, p , 0.05) in shallower water (3 and 7 m merged together)
than at 13 m. In July (Figure 2b), the abundance of round gobies at
3 and 7 m had decreased almost 10-fold from June, and flounders
were more or less evenly distributed at all depths. In September
(Figure 2c), goby densities increased in shallow water when compared with July. The depth distribution of small flounders was
nearly opposite to that of round gobies. Flounder cpue peaked
at 10 m in September where goby cpue was least, resulting in a significant statistical interaction (F1,28 ¼ 12.33; p , 0.0015) in cpue
between species and depth (merging 3 –7 and 10 –13 m depths,
respectively). Overall, merged data of size classes, depths, and
periods showed a negative correlation between round goby and
flounder cpue (log-transformed data, p ¼ 0.044, r ¼ – 0.59).
Diet composition and overlap
The bivalves M. balthica and M. edulis, the polychaete Nereis
diversicolor, and the gastropod Hydrobia sp. were important food
items for all size classes of both species (Table 2). In general, the
most common food item of flounders was M. balthica, constituting some 50% of the diet (shell-free dry weight), and M. edulis
accounted for 30– 50% of the round goby diet. Flounders and
round gobies of corresponding size classes consumed M. balthica
of equal mean size (Figure 3). The size of consumed M. balthica
increased with size class of the fish (ANOVA, F5,184 ¼ 18.456,
p , 0.05), except that there was no significant difference in size
of consumed mussels between small and medium-sized flounders
(p ¼ 0.14). The size of M. edulis consumed also increased with fish
size (Figure 3), but the size differences of mussels consumed were
not significant.
In September, the percentage of M. balthica (mean size
,6 mm; Figure 3) in the diet of small and medium-sized round
gobies increased 10-fold over that in June and July (Table 2).
Simultaneously, the consumption of M. balthica of the same size
(Figure 3) decreased among small flounders (ANOVA,
F2,43 ¼ 5.603, p , 0.05), and there was a non-significant decline
among medium-sized flounders: ANOVA, F1,40 ¼ 2.752, p ¼ 0.105).
There was a significant diet overlap (0.66 + 0.10) between
small flounders and all size classes of gobies in July (low round
goby abundance; Figure 2b). In June and September (high round
goby abundance; Figures 2a and 2c), the value of C between small
Figure 2. Catch rate (cpue) of small, medium-sized, and large
flounders and round gobies in (a) June, (b) July, and (c) September
at different depths (3, 7, 10, 13 m). Note the different scales on
the x-axes.
Figure 3. Sizes of consumed M. balthica and M. edulis for small,
medium, and large flounders (nMacoma¼ 114, nMytilus¼ 24) and
round gobies (nMacoma¼ 76, nMytilus ¼ 110). Mean + s.d.
Competition between non-indigenous round goby and native flounder in the Baltic
483
Figure 4. Proportion of prey items divided into functional groups of
small, medium, and large flounders and round gobies. Also shown
are the values of d15N for flounders and round gobies of different size
classes. Periods (June, July, and September) are merged. Mean + s.d.
flounders and round gobies was significantly lower, (0.36 + 0.17,
ANOVA, F2,8 ¼ 8.07, p , 0.05). Medium-sized and large flounders had values below 0.6 for all periods (0.38 + 0.12), and
there was no significant effect of round goby abundance on diet
overlap (p ¼ 0.14 and 0.64, respectively).
Stable isotope analysis and size-dependent diet shifts
Round gobies and flounders of corresponding size classes were
similarly enriched in d 15N. Although the only significant difference
in d15N enrichment was between large and small gobies (ANOVA,
F2,71 ¼ 6.107, p , 0.01, Figure 4), small fish of both species tended
to be more enriched than large and medium-sized fish. Prey organisms for all sampling periods (June, July, and September)
were divided into functional groups according to Wiktor
(1985; Figure 4): suspension-feeders (M. edulis, Cardium sp.,
and Balanus improvisus), facultative suspension/deposit-feeders
(M. balthica, Mya arenaria), deposit-feeders (N. diversicolor,
Hydrobia sp, Gammarus sp., and Corophium sp.), and fish
(Gasterosteus aculeatus). The importance of N. diversicolor in the
diet decreased significantly with increased fish size for round
gobies and flounders (Mann –Whitney U-test, p , 0.05 for both
species, Figure 4). Concurrently, the proportion of suspensionfeeders and facultative suspension/deposit-feeders (M. edulis and
M. balthica, respectively) in the diet increased with fish size
(Mann –Whitney U-test, p , 0.05).
Prey preference
Flounders of all sizes seemed to prefer M. balthica to M. edulis,
whereas round gobies, irrespective of size class, did not discriminate between prey species (Figure 5). Small (n ¼ 8) and mediumsized (n ¼ 6) flounders exhibited significantly greater positive
selection for small- and medium-sized M. balthica, respectively,
than for M. edulis of similar size (ANOVA: F1,5 ¼ 6.441,
p , 0.05; F1,7 ¼ 4.945, p , 0.05). Small round gobies (n ¼ 9)
selected small mussels, and medium-sized gobies (n ¼ 9) selected
both small and medium-sized mussels. Large gobies (n ¼ 10) ate
all mussels available. Just two large flounders consumed mussels
during the experimental period.
Figure 5. Selection index of (a) small, (b) medium-sized, and (c)
large M. balthica and M. edulis for small, medium, and large flounders
and round gobies. Values above the horizontal line indicate selection
for species and size of mussel. Mean + s.e.
Discussion
The results indicate that round gobies have the potential to impact
flounder habitat and food resource utilization in a negative
manner. Catch data showed reverse depth distributions of round
gobies and flounders when round gobies were abundant, and
that total abundance of the two species was negatively correlated.
At times of high round goby abundance, flounder depth distribution was constrained to deeper areas (10 and 13 m), but when
round goby abundance was low, as in July, flounders were found
at all depths. The great abundance of round gobies in shallower
water in June possibly reflects a migration from wintering habitats
to shallower waters further into Puck Bay (Figure 1). In July, the
small catch of round gobies also at the shallow sampling station
(3 m) suggests that spawning was taking place in even shallower
water (,1.5 m, not sampled) on rocky and stony substrata close
to the shore (Moskal’kova, 1996; Pinchuk et al., 2003). The availability of nesting sites is limited in the Gulf of Gdańsk (Sapota,
2004), and at Oksywie the main rocky habitat is restricted to the
artificial stonewall at the shore. Studies from the North
American Great Lakes have shown that round gobies are aggressive
and territorial (Dubs and Corkum, 1996; Janssen and Jude, 2001;
Balshine et al., 2005), and that behavioural interaction between
species is likely. Therefore, it is reasonable to suggest that
484
reduced abundance of gobies at the depths sampled in July made
the habitat more available for flounders. Alternative explanations
to such habitat partitioning between the species, e.g. differences
in migratory patterns, temperature preferences, predation, and/
or depth-dependent distribution of preferred food items, are less
plausible. Flounders migrate between the coast and offshore
to feed and to spawn, respectively. In the Gdańsk deep, they
spawn in early spring (February– mid-April), then return to
shallower water in May (Cie˛glewicz, 1947; Molander, 1964;
I. Psuty-Lipska, Sea Fisheries Institute Gdynia, pers. comm.).
Hence, flounders were likely inhabiting the shallow water well
before our sampling in June. Nor can possible differences in temperature preference between species explain the depth partitioning
we observed in June, because flounders were evenly distributed
over all depths in July, when temperature was considerably
higher. As the sampled area was almost devoid of predatory fish
such as cod and perch (AMLK and GA, pers. obs.), predation
cannot explain the abundance and depth distribution patterns.
In terms of food distribution, Wiktor (1985) found that
M. balthica, which was selected more by flounders than was
M. edulis in the preference experiment, constituted more of the
bottom fauna at 3 –5 m than at 8 – 10 m.
Results from stomach analyses and the prey preference experiment showed that both species fed extensively on bivalves, and
that fish with similar gape size selected bivalves of similar size.
The prey preference experiment clearly showed that flounders
preferred M. balthica whereas round gobies exhibited a wider preference of bivalves. As M. balthica constituted some 50% of flounder diet, we infer that flounders depend largely on that species. The
results from the stomach content analyses and experimental food
preference studies may have been biased by species-dependent
differences in the intestines, evacuation rates, and behaviour.
Also, the importance of some prey items that were well digested
could have been over- or underestimated. Consumption of
N. diversicolor could have been overestimated because the bristles
may remain in the stomach for a long time. In contrast, bivalve
consumption could have been underestimated because round
gobies at least might swallow only the flesh and not the shells.
However, these issues are probably of minor importance,
because all bivalves consumed in the prey preference experiment
were swallowed whole. For large fish, the selection results are
not clear, partly because large flounders seemed to be less easily
acclimatized to laboratory conditions than gobies (only 2 of 10
fish foraged). Prey depletion attributable to limited prey offered
in relation to foraging time precluded conclusions about food
preferences for large gobies.
It could be argued that high goby abundances may result in
local depletion of preferred food items for flounders (specifically
M. balthica), so affecting its habitat distribution. In the
Laurentian Great Lakes, Kuhns and Berg (1999) showed that
round gobies were able to reduce significantly the densities of
benthic invertebrates. For flounders, M. balthica is more efficiently
digested than other shelled food items, because it does not survive
the passage through the gut (Aarnio and Bonsdorff, 1997).
However, in September, the percentage of M. balthica in the diet
of small flounders was considerably less than in June and July,
whereas M. balthica of the same size (Figure 3) increased 10-fold
in the diet of small and medium-sized round gobies (Table 2).
The lesser proportion of such high-energy food in the diet of
small flounders indicates a competition-induced shift to suboptimal food resources.
A. M. L. Karlson et al.
The decline of native benthic fish populations in the Great
Lakes has been related to round goby predation on early life
stages of native fish (French and Jude, 2001). As roe and fish constitute only a minor part of the diet of round gobies, it is likely that
goby-induced declines of native species in the Baltic Sea would be
more by competition than by predation.
The recently invaded non-indigenous polychaete Marenzelleria
viridis was not observed in any fish stomach, although the species
is reported from the area (Zmudzinski et al., 1997).
The similarities in diet composition between round gobies and
flounders were supported by comparable d 15N values, suggesting
that fish of both species with similar gape size share the same
trophic level. A consumer is enriched in 15N with 3 –4‰ relative
to its diet (Owens, 1987), so the 15N value reflects the importance
of prey items with different 15N values consumed. Hence, the 15N
enrichment in an animal’s tissue can be used as a proxy for trophic
level. Stable nitrogen isotopes also prove a good indicator of diet
change during ontogeny (Gaines et al., 2002; Cocheret de la
Moriniere et al., 2003). Interestingly, the d 15N value decreased
with size for both species. This is in contrast to commonly
reported ontogenetic development, i.e. trophic level of a species
increases with size (France et al., 1998; Gaines et al., 2002;
Cocheret de la Moriniere et al., 2003), because body size determines the range of prey sizes a predator is able to consume
(Cohen et al., 1993). From this analysis, we deduce that small
fish consumed more deposit-feeders, especially N. diversicolor,
than larger fish (Figure 4). Deposit-feeders are generally more
enriched in 15N than suspension-feeding bivalves, which assimilate
pelagic phytoplankton (Kang et al., 2003). The d 15N value of
N. diversicolor is significantly higher than that of the bivalve
M. edulis in the northern Baltic (R. Neidemann, Stockholm
University, pers. comm.). In support of the nitrogen isotope signatures, feeding on bivalves by both species investigated here
increased with size of fish, indicating an ontogenetic diet shift in
both species, as suggested by Skóra and Rzeznik (2001) and
Jennings et al. (2001). However, a high d 15N value may also indicate starvation (Haubert et al., 2005) and a competition-induced
shift to suboptimal food resources in the diet of small flounders
could possibly result in starvation.
The diet similarities suggest a potential for food competition to
develop, if resources become limiting. Nevertheless, because of
opposite seasonal peaks in consumption of important food
items, the diet overlap was low to moderate on all sampling
occasions and combinations of size classes. However, significant
overlap was noted between small flounders and all size classes of
round gobies in July, when the abundance of the latter species
was at its lowest and flounders were evenly distributed at all
depths. This interaction between diet overlap and round goby
abundance is important, because it suggests that high round
goby abundance can restrict flounder habitat utilization and
thereby also food availability for the latter species. In addition to
heavy fishing pressure (Psuty-Lipska, 2001; Draganik and
Psuty-Lipska, 2002), limited food resources may have negative
local effects on the flounder population. Our results therefore
support what many authors have suggested before, that round
gobies compete with flounders for resources.
Acknowledgements
The work was carried out under the framework of the Swedish
programme AquAliens, funded by the Swedish EPA. The
Swedish Board of Fisheries also contributed financially to the
Competition between non-indigenous round goby and native flounder in the Baltic
study. We thank M. Koźbiał, M. Skóra, T. Kakareko, and students
from the University of Gdańsk for valuable help in the field.
Experienced fishers in Oksywie, especially S. Siewiert, were very
supportive during sampling. We also acknowledge R. Koza and
other staff at Hel Marine Station for their help with logistics,
and B. Arciszewski, A. Strandmark, and G. Hugelius for support
with the laboratory experiments. Finally, we thank S. Hansson,
O. Hjerne, E. Gorokhova, S. Pakkasmaa, and R. Elmgren for constructive comments on very early versions, and S. Olenin and an
anonymous reviewer for helpful and important comments on
the submitted version of the work.
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